Eur. J. Entomol. 121: 310-323, 2024 | DOI: 10.14411/eje.2024.033
Transcriptome analysis reveals glycometabolism and antioxidation-related genes involved in the antifungal immune response of Spodoptera frugiperda larvae against Beauveria bassiana infectionOriginal article
- 1 Institute of Nanfan & Seed Industry, Guangdong Academy of Sciences, Guangzhou, 510316, China; e-mail: liujb5@mail3.sysu.edu.cn
- 2 Key Laboratory of Sugarcane Biotechnology and Genetic Improvement (Guangxi), Ministry of Agriculture and Rural Affairs/Guangxi Key Laboratory of Sugarcane Genetic Improvement/Sugarcane Research Institute, Guangxi Academy of Agricultural Sciences, Nanning, 530007, China; e-mail: qinzqcn@163.com
Spodoptera frugiperda damages crops around the world and has developed resistance to many pesticides. Beauveria bassiana, a fungus that is harmless to humans and the environment, is widely used in pest control. In our study, differentially expressed genes between S. frugiperda larvae, both exposed and unexposed, to B. bassiana were analyzed by transcriptome sequencing. More than 160 Gb of clean data were obtained, and 2767 and 2892 DEGs were identified in LH36vsCK36 and LH144vsCK144, respectively. To explore the roles of glycometabolism and antioxidation-related enzyme genes in S. frugiperda against B. bassiana infection, the expression patterns of those genes when under attack from B. bassiana were analyzed by quantitative real-time PCR. The results of enzyme activity experiments revealed that S. frugiperda larvae exposed to B. bassiana could upregulate these genes to produce more enzymes related to the maintainance of normal glucose metabolism, as well as regulate the expression of detoxification and antioxidant factors to enhance the larvae's detoxification and antioxidant capacity. The result implied that glycometabolism and antioxidation-related enzymes and genes played critical roles in the antifungal immune process of S. frugiperda larvae. This study enhances our understanding of the molecular mechanisms related to regulation of metabolism and provides a basis for exploring new methods to combat antifungal resistance in S. frugiperda.
Keywords: Lepidoptera, Noctuidae, pest, bio-insecticide, agriculture, carbohydrates, REDOX enzyme system, gene expression
Received: January 31, 2024; Revised: August 12, 2024; Accepted: August 12, 2024; Published online: September 11, 2024 Show citation
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References
- Aioub A.A.A., Hashem A.S., El-Sappah A.H., El-Harairy A., Abdel-Hady A.A.A., Al-Shuraym L.A., Sayed S., Huang Q. & Abdel-Wahab S.I.Z. 2023: Identification and characterization of glutathione S-transferase genes in Spodoptera frugiperda (Lepidoptera: Noctuidae) under insecticides stress. - Toxics 11: 542, 16 pp.
Go to original source...
- Carla H.B., Flavia R.S., Gabriel M.M., Marianela S., Everton K.K. & Nicolas P. 2019: The entomopathogenic fungus Beauveria bassiana produces microsclerotia-like pellets mediated by oxidative stress and peroxisome biogenesis. - Environ. Microbiol. Rep. 11: 518-524.
Go to original source...
- Celar F.A. & Kos K. 2016: Effects of selected herbicides and fungicides on growth, sporulation and conidial germination of entomopathogenic fungus Beauveria bassiana. - Pest Manag. Sci. 72: 2110-2117.
Go to original source...
- Dalton T.P., Shertzer H.G. & Puga A. 1999: Regulation of gene expression by reactive oxygen. - Annu. Rev. Pharmacol. Toxicol. 39: 67-101.
Go to original source...
- Dejong R.J., Miller L.M., Molina-Cruz A., Gupta L., Kumar S. & Barillas-Mury C. 2007: Reactive oxygen species detoxification by catalase is a major determinant of fecundity in the mosquito Anopheles gambiae. - Proc. Natl. Acad. Sci. USA 104: 2121-2126.
Go to original source...
- Duncan D.M., Kiefel P. & Duncan I. 2017: Mutants for Drosophila isocitrate dehydrogenase 3b are defective in mitochondrial function and larval cell death. - G3 / Genes Genom. Genet. 7: 789-799.
Go to original source...
- Grabherr M.G., Haas B.J., Yassour M., Levin J.Z., Thompson D.A., Amit I., Adiconis X., Fan L., Raychowdhury R., Zeng Q. et al. 2011: Full-length transcriptome assembly from RNA-Seq data without a reference genome. - Nat. Biotechnol. 29: 644-652.
Go to original source...
- Gullner G., Komives T., Király L. & Schröder P. 2018: Glutathione S-transferase enzymes in plant-pathogen interactions. - Front. Plant Sci. 9: 1836, 19 pp.
Go to original source...
- Han J., Won E.J., Hwang D.S., Rhee J.S., Kim I.C. & Lee J.S. 2013: Effect of copper exposure on GST activity and on the expression of four GSTs under oxidative stress condition in the monogonont rotifer, Brachionus koreanus. - Comp. Biochem. Phys. (C) 158: 91-100.
Go to original source...
- Hong S., Shang J., Sun Y., Tang G. & Wang C. 2024: Fungal infection of insects: molecular insights and prospects. - Trends Microbiol. 32: 302-316.
Go to original source...
- Hu N., Dong Z.Q., Long J.Q., Zheng N., Hu C.W., Wu Q., Chen P., Lu C. & Pan M.H. 2021: Transcriptome analysis reveals changes in silkworm energy metabolism during Nosema bombycis infection. - Pestic. Biochem. Physiol. 174: 104809, 13 pp.
Go to original source...
- Jabbour R., Crowder D.W., Aultman E.A. & Snyder W.E. 2011: Entomopathogen biodiversity increases host mortality. - Biol. Control 59: 277-283.
Go to original source...
- Jia M., Cao G.C., Li Y.B., Tu X.B., Wang G.J., Nong X.Q., Whitman D.W. & Zhang Z.H. 2016: Biochemical basis of synergism between pathogenic fungus Metarhizium anisopliae and insecticide chlorantraniliprole in Locusta migratoria (Meyen). - Sci. Rep. 6: 28424, 15 pp.
Go to original source...
- Kanehisa M., Araki M., Goto S., Hattori M., Hirakawa M., Itoh M., Katayama T., Kawashima S., Okuda S., Tokimatsu T. & Yamanishi Y. 2008: KEGG for linking genomes to life and the environment. - Nucl. Acids Res. 36: 480-484.
Go to original source...
- Kolawole A.O., Olajuyigbe F.M., Ajele J.O. & Adedire C.O. 2014: Activity of the antioxidant defense system in a typical bioinsecticide-and synthetic insecticide-treated cowpea storage beetle Callosobrochus maculatus F. (Coleoptera: Chrysomelidae). - Int. J. Insect Sci. 6: 99-108.
Go to original source...
- Kshatriya K. & Gershenzon J. 2024: Disarming the defenses: Insect detoxification of plant defense-related specialized metabolites. - Curr. Opin. Plant Biol. 81: 102577, 8 pp.
Go to original source...
- Li Z.Z., Alves S.B., Roberts D.W., Fan M.Z., Delalibera I., Tang J., Lopes R.B., Faria M. & Rangel D.E.N. 2010: Biological control of insects in Brazil and China: history, current programs and reasons for their successes using entomopathogenic fungi. - Biocontrol Sci. Techn. 20: 117-136.
Go to original source...
- Liu H., Zhao X., Guo M., Liu H. & Zheng Z. 2015: Growth and metabolism of Beauveria bassiana spores and mycelia. -BMC Microbiol. 15: 267, 12 pp.
Go to original source...
- Livak K.J. & Schmittgen T.D. 2001: Analysis of relative gene expression data using real-time quantitative PCR and the 2-ΔΔCt method. - Methods 25: 402-408.
Go to original source...
- Long D.M., Frame A.K., Reardon P.N., Cumming R.C., Hendrix D.A., Kretzschmar D. & Giebultowicz J.M. 2020: Lactate dehydrogenase expression modulates longevity and neurodegeneration in Drosophila melanogaster. - Aging (Albany) 12: 10041-10058.
Go to original source...
- Martinelli S., Barata R.M., Zucchi M.I., Silva-Filho M. de C. & Omoto C. 2006: Molecular variability of Spodoptera frugiperda (Lepidoptera: Noctuidae) populations associated to maize and cotton crops in Brazil. - J. Econ. Entomol. 99: 519-526.
Go to original source...
- Mascarin G.M. & Jaronski S.T. 2016: The production and uses of Beauveria bassiana as a microbial insecticide. - World J. Microb. Biotechnol. 32: 177, 26 pp.
Go to original source...
- Maurya R. & Namdeo M. 2022: Superoxide dismutase: A key enzyme for the survival of intracellular pathogens in host. In Ahmad R. (ed.): Reactive Oxygen Species. IntechOpen, URL: http://dx.doi.org/10.5772/intechopen.100322.
Go to original source...
- Nyathi Y. & Baker A. 2006: Plant peroxisomes as a source of signalling molecules. - Biochem. Biophys. Acta / Mol. Cell Res. 1763: 1478-1495.
Go to original source...
- Ortiz-Urquiza A., Riveiro-Miranda L., Santiago-Álvarez C. & Quesada-Moraga E. 2010: Insect-toxic secreted proteins and virulence of the entomopathogenic fungus Beauveria bassiana. - J. Invertebr. Pathol. 105: 270-278.
Go to original source...
- Patel M.S., Nemeria N.S., Furey W. & Jordan F. 2014: The pyruvate dehydrogenase complexes: structure-based function and regulation. - J. Biol. Chem. 289: 16615-16623.
Go to original source...
- Pertea G., Huang X., Liang F., Antonescu V., Sultana R., Karamycheva S., Lee Y., White J., Cheung F., Parvizi B., Tsai J. & Quackenbush J. 2003: TIGR Gene Indices clustering tools (TGICL): a software system for fast clustering of large EST datasets. - Bioinformatics 19: 651-652.
Go to original source...
- Quackenbush J., Cho J., Lee D., Liang F., Holt I., Karamycheva S., Parvizi B., Pertea G., Sultana R. & White J. 2001: The TIGR Gene Indices: analysis of gene transcript sequences in highly sampled eukaryotic species. - Nucl. Acids Res. 29: 159-164.
Go to original source...
- Ramos Y., Portal O., Lysoe E., Meyling N.V. & Klingen I. 2017: Diversity and abundance of Beauveria bassiana in soils, stink bugs and plant tissues of common bean from organic and conventional fields. - J. Invertebr. Pathol. 150: 114-120.
Go to original source...
- Rhee S.G. 2006: H2O2, a necessary evil for cell signaling. - Science 312: 1882-1883.
Go to original source...
- Rubio R.O., Suzuki A., Mitsumasu K., Homma T., Niimi T., Yamashita O. & Yaginuma T. 2011: Cloning of cDNAs encoding sorbitol dehydrogenase-2a and b, enzymatic characterization, and up-regulated expression of the genes in Bombyx mori diapause eggs exposed to 5°C. - Insect Biochem. Molec. 41: 378-387.
Go to original source...
- Sezer B. & Ozalp P. 2015: Effect of juvenile hormone analogue, pyriproxyfen on antioxidant enzymes of greater wax moth, Galleria mellonella (Lepidoptera: Pyralidae: Galleriinae) larvae. - Pak. J. Zool. 47: 665-669.
- Shimozawa Y., Matsuhisa H., Nakamura T., Himiyama T. & Nishiya Y. 2022: Reducing substrate inhibition of malate dehydrogenase from Geobacillus stearothermophilus by C-terminal truncation. - Protein Eng. Des. Sel. 35: gzac008, 7 pp.
Go to original source...
- Stephenie S., Chang Y.P., Gnanasekaran A., Esa N.M. & Gnanaraj C. 2020: An insight on superoxide dismutase (SOD) from plants for mammalian health enhancement. - J. Funct. Foods 68: 103917, 10 pp.
Go to original source...
- Strange R.C., Spiteri M.A., Ramachandran S. & Fryer A.A. 2001: Glutathione-S-transferase family of enzymes. - Mutat. Res. 482: 21-26.
Go to original source...
- Sun R., Hong B., Reichelt M., Luck K., Mai D.T., Jiang X., Gershenzon J. & Vassao D.G. 2023: Metabolism of plant-derived toxins from its insect host increases the success of the entomopathogenic fungus Beauveria bassiana. - ISME J. 17: 1693-1704.
Go to original source...
- Tian Z.L., Ruan C.C., Li Q.Y., Tan Y.F. & Sun G.Z. 2008: Advances in studies on the pathogenic mechanism of Beauveria bassiana to insects. - J. Anhui Agric. Sci. 36: 16000-16002.
- Todd E.L. & Poole R.W. 1980: Keys and illustrations for the armyworm moths of the noctuid genus Spodoptera Guenée from the western hemisphere. - Ann. Entomol. Soc. Am. 6: 722-738.
Go to original source...
- Vommaro M.L., Zanchi C., Angelone T., Giglio A. & Kurtz J. 2023: Herbicide exposure alters the effect of the enthomopathogen Beauveria bassiana on immune gene expression in mealworm beetles. - Environ. Pollut. 338: 122662, 10 pp.
Go to original source...
- Wang C.S. & Feng M.G. 2014: Advances in fundamental and applied studies in China of fungal biocontrol agents for use against arthropod pests. - Biol. Control 68: 129-135.
Go to original source...
- Wang T., Hou M., Zhao N., Chen Y.F., Lv Y., Li Z.R., Zhang R., Xin W.T., Zou X.Y. & Hou L. 2013: Cloning and expression of the sorbitol dehydrogenase gene during embryonic development and temperature stress in Artemia sinica. - Gene 521: 296-302.
Go to original source...
- Wang H., Peng H., Li W., Cheng P. & Gong M. 2021: The toxins of Beauveria bassiana and the strategies to improve their virulence to insects. - Front. Microbiol. 12: 705343, 11 pp.
Go to original source...
- Welinder K.G. 1992: Superfamily of plant, fungal and bacterial peroxidases. - Curr. Opin. Struc. Biol. 2: 388-393.
Go to original source...
- Wu J., Tang W., Li Z., Chakraborty A., Zhou C., Li F. & He S. 2024: Duplications and losses of the detoxification enzyme Glycosyltransferase 1 are related to insect adaptations to plant feeding. - Int. J. Mol. Sci. 25: 6080, 16 pp.
Go to original source...
- Xia H., Wu C., Xu Q., Shi J., Feng F., Chen K., Yao Q., Wang Y. & Wang L. 2011: Molecular cloning and characterization of lactate dehydrogenase gene 1 in the silkworm, Bombyx mori. - Mol. Biol. Rep. 38: 1853-1860.
Go to original source...
- Xu W.S., Hu M.Y. & Zhong G.H. 2005: The studies of mycotoxins as pesticides in agriculture pests control. - J. Yunnan Agr. Univ. 20: 339-342.
- Ye J., Fang L., Zheng H., Zhang Y., Chen J., Zhang Z., Wang J., Li S., Li R., Bolund L. & Wang J. 2006: WEGO: a web tool for plotting GO annotations. - Nucl. Acids Res. 34: 293-297.
Go to original source...
- Yu S.J. 2004: Detoxification mechanisms in insects. In Capinera L.J. (ed.): Encyclopedia of Entomology. Springer, Dordrecht, pp. 687-699.
Go to original source...
- Zeinali F., Homaei A. & Kamrani E. 2015: Sources of marine superoxide dismutases: Characteristics and applications. - Int. J. Biol. Macromol. 79: 627-637.
Go to original source...
- Zhang C., Teng B., Liu H., Wu C., Wang L. & Jin S. 2023: Impact of Beauveria bassiana on antioxidant enzyme activities and metabolomic profiles of Spodoptera frugiperda. - J. Invertebr. Pathol. 198: 107929, 11 pp.
Go to original source...
- Zhao Z.C. 1981: Studies on the pathogenesis of Beauveria bassiana. - Chin. J. Prev. Med. 15: 272-274 [in Chinese].
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